Skip to main content
Log in

Meiotic differentiation during colony maturation in Sacchatomyces cerevisiae

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

As yeast colonies ceased growth, cells at the edge of these colonies transited from the cell division cycle into meiosis at high efficiency. This transition occurred remarkably synchronously and only at late stages of colony maturation. The transition occurred on medium containing acetate or low concentrations of glucose, but not on medium containing high glucose. The repression by high glucose was overcome when IME1 was overexpressed from a plasmid. Experiments with different growth media imply that meiosis in colonies is triggered by changes in the nutrient environment as colonies mature. HAP2 is required to sporulate in any carbon source, whereas GRR1 is required for glucose repression of sporulation. CLN3 is required to repress meiosis in colonies but not in liquid cultures, indicating that the regulators that mediate the transition to meiosis in colonies are not identical to the regulators that mediate this transition in liquid cultures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bernard F, Andre B (2001) Ubiquitin and the SCF(Grrl) ubiquitin ligase complex are involved in the signaling pathway activated by external amino acids in Saccharomyces cerevisiae. FEBS Lett 496:81–85

    Article  PubMed  CAS  Google Scholar 

  • Blacketer MJ, Madaule P, Myers AM (1995) Mutational analysis of morphologic differentiation in Saccharomyces cerevisiae. Genetics 140:1259–1275

    PubMed  CAS  Google Scholar 

  • Briza P, Ellinger A, Winkler G, Breitenbach M (1988) Chemical composition of the yeast ascospore wall. The second outer layer consists of chitosan. J Biol Chem 263:11569–11574

    PubMed  CAS  Google Scholar 

  • Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998) The transcriptional program of sporulation in budding yeast. Science 282:699–705

    Article  PubMed  CAS  Google Scholar 

  • Colomina N, Gari E, Gallego C, Herrero E, Aldea M (1999) Gl cyclins block the Imel pathway to make mitosis and meiosis incompatible in budding yeast. EMBO J 18:320–329

    Article  PubMed  CAS  Google Scholar 

  • Dang VD, Valens M, Bolotin-Fukuhara M, Daignan-Fornier B (1994) A genetic screen to isolate genes regulated by the yeast CCAAT-box binding protein Hap2p. Yeast 10:1273–1283

    Article  PubMed  CAS  Google Scholar 

  • Erdman S, Snyder M (2001) A filamentous growth response mediated by the yeast mating pathway. Genetics 159:919–928

    PubMed  CAS  Google Scholar 

  • Gancedo JM (2001) Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiol Rev 25:107–123

    Article  PubMed  CAS  Google Scholar 

  • Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077–1090

    Article  PubMed  CAS  Google Scholar 

  • Gray M, Honigberg SM (2001) Effect of chromosomal locus, GC content and length of homology on PCR-mediated targeted gene replacement in Saccharomyces. Nucleic Acids Res 29:5156–5162

    Article  PubMed  CAS  Google Scholar 

  • Guarente L, Lalonde B, Gifford P, Alani E (1984) Distinctly regulated tandem upstream activation sites mediate catabolite repression of the CYC1 gene of S. cerevisiae. Cell 36:503–511

    Article  PubMed  CAS  Google Scholar 

  • Hayashi M, Ohkuni K, Yamashita I (1998) Control of division arrest and entry into meiosis by extracellular alkalization in Saccharomyces cerevisiae. Yeast 14:905–913

    Article  PubMed  CAS  Google Scholar 

  • Honigberg SM, Lee RH (1998) Snfl kinase connects nutritional pathways controlling meiosis in Saccharomyces cerevisiae. Mol Cell Biol 18:4548–4555

    PubMed  CAS  Google Scholar 

  • Honigberg SM, McCarroll RM, Esposito RE (1993) Regulatory mechanisms in meiosis. Curr Opin Cell Biol 5:219–225

    Article  PubMed  CAS  Google Scholar 

  • Johnston M, Carlson M (1992) Regulation of carbon and phosphate utilization. In: Jones EW, Pringle JR, Broach JR (eds) The molecular and cellular biology of the yeast Saccharomyces: gene expression. Cold Spring Harbor Laboratory Press, Plain-view, N.Y., pp 193–282

    Google Scholar 

  • Kappeli O (1986) Regulation of carbon metabolism in Saccharomyces cerevisiae and related yeasts. Adv Microb Physiol 28:181–209

    Article  PubMed  CAS  Google Scholar 

  • Kassir Y, Granot D, Simchen G (1988) IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell 52:853–862

    Article  PubMed  CAS  Google Scholar 

  • Kupiec M, Byers B, Esposito RE, Mitchell AP (1997) Meiosis and sporulation in Saccharomyces cerevisiae. In: Pringle JR, Broach JR, Jones EW (eds) The molecular and cellular biology of the yeast Saccharomyces: cell cycle and cell biology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 889–1036

    Google Scholar 

  • Lee RH, Honigberg SM (1996) Nutritional regulation of late meiotic events in Saccharomyces cerevisiae through a pathway distinct from initiation. Mol Cell Biol 16:3222–3232

    PubMed  CAS  Google Scholar 

  • Li FN, Johnston M (1997) Grrl of Saccharomyces cerevisiae is connected to the ubiquitin proteolysis machinery through Skpl: coupling glucose sensing to gene expression and the cell cycle. EMBO J 16:5629–5638

    Article  PubMed  CAS  Google Scholar 

  • Loeb JD, Kerentseva TA, Pan T, Sepulveda-Becerra M, Liu H (1999) Saccharomyces cerevisiae Gl cyclins are differentially involved in invasive and pseudohyphal growth independent of the filamentation mitogen-activated protein kinase pathway. Genetics 153:1535–1546

    PubMed  CAS  Google Scholar 

  • Meunier JR, Choder M (1999) Saccharomyces cerevisiae colony growth and aging: biphasic growth accompanied by changes in gene expression. Yeast 15:1159–1169

    Article  PubMed  CAS  Google Scholar 

  • Minarikova L, Kuthan M, Ricicova M, Forstova J, Palkova Z (2001) Differentiated gene expression in cells within yeast colonies. Exp Cell Res 271:296–304

    Article  PubMed  CAS  Google Scholar 

  • Mitchell AP (1994) Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev 58:56–70

    PubMed  CAS  Google Scholar 

  • Ohkuni K, Hayashi M, Yamashita I (1998) Bicarbonate-mediated social communication stimulates meiosis and sporulation of Saccharomyces cerevisiae. Yeast 14:623–631

    Article  PubMed  CAS  Google Scholar 

  • Palkova Z, Forstova J (2000) Yeast colonies synchronize their growth and development. J Cell Sci 113:1923–1928

    PubMed  CAS  Google Scholar 

  • Patton EE, Willems AR, Sa D, Kuras L, Thomas D, Craig KL, Tyers M (1998) Cdc53 is a scaffold protein for multiple Cdc34/ Skpl/F-box protein complexes that regulate cell division and methionine biosynthesis in yeast. Genes Dev 12:692–705

    Article  PubMed  CAS  Google Scholar 

  • Primig M, Williams RM, Winzeler EA, Tevzadze GG, Conway AR, Hwang SY, Davis RW, Esposito RE (2000) The core meiotic transcriptome in budding yeasts. Nat Genet 26:415–423

    Article  PubMed  CAS  Google Scholar 

  • Purnapatre K, Piccirillo S, Schneider BL, Honigberg SM (2002) The CLN3/SWI6/CLN2 pathway and SNF1 act sequentially to regulate meiotic initiation in Saccharomyces cerevisiae. Genes Cells 7:675–691

    Article  PubMed  CAS  Google Scholar 

  • Rose MD, Winston F, Hieter P. (1990). Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Rua D, Tobe BT, Kron SJ (2001) Cell cycle control of yeast filamentous growth. Curr Opin Microbiol 4:720–727

    Article  PubMed  CAS  Google Scholar 

  • Scherz R, Shinder V, Engelberg D (2001) Anatomical analysis of Saccharomyces cerevisiae stalk-like structures reveals spatial organization and cell specialization. J Bacteriol 183:5402–5413

    Article  PubMed  CAS  Google Scholar 

  • Shapiro JA (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104

    Article  PubMed  CAS  Google Scholar 

  • Smith HE, Mitchell AP (1989) A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol 9:2142–2152

    PubMed  CAS  Google Scholar 

  • Smith HE, Driscoll SE, Sia RA, Yuan HE, Mitchell AP (1993) Genetic evidence for transcriptional activation by the yeast IME1 gene product. Genetics 133:775–784

    PubMed  CAS  Google Scholar 

  • Treinin M, Simchen G (1993) Mitochondrial activity is required for the expression of IM El, a regulator of meiosis in yeast. Curr Genet 23:223–227

    Article  PubMed  CAS  Google Scholar 

  • Vidan S, Mitchell AP (1997) Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim l5p. Mol Cell Biol 17:2688–2697

    PubMed  CAS  Google Scholar 

  • Wendland J (2001) Comparison of morphogenetic networks of filamentous fungi and yeast. Fungal Genet Biol 34:63–82

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Saul M. Honigberg.

Additional information

Communicated by S. Hohmann

Published online: 11 October 2002

Rights and permissions

Reprints and permissions

About this article

Cite this article

Purnapatre, K., Honigberg, S.M. Meiotic differentiation during colony maturation in Sacchatomyces cerevisiae . Curr Genet 42, 1–8 (2002). https://doi.org/10.1007/s00294-002-0331-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-002-0331-x

Keywords

Navigation